Methane assimilation and trophic interactions with marine Methylomicrobium in deep-water coral reef sediment off the coast of Norway

Jensen, Sigmund; Neufeld, Josh D.; Birkeland, Nils Kåre; Hovland, Martin; Murrell, J. Colin

doi:10.1111/j.1574-6941.2008.00575.x

Cited by 43 publications

(33 citation statements)

References 59 publications

(109 reference statements)

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“…In addition, although cultured members of the Methylophilaceae and Methylophaga spp. are known to oxidize methanol but not methane, isotope tracer experiments have consistently shown that these groups incorporate 13 C from 13 CH 4 , presumably through crossfeeding on methanol released by methanotrophs, to the extent that methylotroph sequences can outnumber Methylococcaceae sequences in 13 Clabeled DNA (16)(17)(18). We thus find the change in microbial community composition to be consistent with a methanotrophic bloom between June and September 2010.…”

supporting

confidence: 54%

Response to Comment on “A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico”

Kessler

Valentine

Redmond

et al. 2011

Science

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We hypothesized that methane from the Deepwater Horizon oil spill was quantitatively consumed and presented results from four tests supporting this finding. Subsequent published studies provide further support for our conclusions. We refute the criticisms by Joye et al., which are incorrect, internally contradictory, based on flow-rate estimates that exceed consensus values, and overall do not disprove our hypothesis or invalidate its underlying assumptions.

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supporting

confidence: 54%

Response to Comment on “A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico”

Kessler

Valentine

Redmond

et al. 2011

Science

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“…Flavobacteria in particular were more abundant in plume samples than nonplume samples (10-35% of sequences vs. 1-15%). Flavobacteria are abundant in the ocean and are often associated with the degradation of high molecular weight dissolved organic carbon compounds (23), but several methanol-oxidizing strains of Flavobacterium have been isolated (24) and they have often been observed in 13 C-labeled DNA from methane SIP studies (25). The Flavobacteria may therefore have been secondary consumers of methane, oil, or cellular decay products.…”

mentioning

confidence: 99%

“…Given that the cultivated strains of Colwellia are capable of degrading many different carbon sources (33,40), either explanation is possible. It is also important to note that we cannot exclude the possibility of cross-feeding (25,39), whereby one organism is responsible for the initial oxidation step (e.g., ethane to ethanol) and a different organism then consumes this 13 C-labeled intermediate (e.g., ethanol) and incorporates it into 13 C biomass. However, given the dominance of Colwellia in the SIP samples and the high rates of ethane and propane oxidation in June, when Colwellia sequences accounted for approximately 70% of sequences in plume samples (2), it is likely that Colwellia was responsible for the bulk of ethane and propane oxidation in situ, although the SIP results show the DWH Oceanospirillales may also have played a role.…”

mentioning

confidence: 99%

Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill

Redmond

Valentine

2011

Proc. Natl. Acad. Sci. U.S.A.

342

379

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Microbial communities present in the Gulf of Mexico rapidly responded to the Deepwater Horizon oil spill. In deep water plumes, these communities were initially dominated by members of Oceanospirillales, Colwellia, and Cycloclasticus. None of these groups were abundant in surface oil slick samples, and Colwellia was much more abundant in oil-degrading enrichment cultures incubated at 4°C than at room temperature, suggesting that the colder temperatures at plume depth favored the development of these communities. These groups decreased in abundance after the well was capped in July, but the addition of hydrocarbons in laboratory incubations of deep waters from the Gulf of Mexico stimulated Colwellia's growth. Colwellia was the primary organism that incorporated 13 C from ethane and propane in stable isotope probing experiments, and given its abundance in environmental samples at the time that ethane and propane oxidation rates were high, it is likely that Colwellia was active in ethane and propane oxidation in situ. Colwellia also incorporated 13 C benzene, and Colwellia's abundance in crude oil enrichments without natural gas suggests that it has the ability to consume a wide range of hydrocarbon compounds or their degradation products. However, the fact that ethane and propane alone were capable of stimulating the growth of Colwellia, and to a lesser extent, Oceanospirillales, suggests that high natural gas content of this spill may have provided an advantage to these organisms. methane | biodegradation | marine bacteria | archaea | alkane

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“…methanotrophs co-occur with other nonmethanotrophic bacteria and function collectively with them as a community to consume methane (18)(19)(20)(21)(22)(23)(24)(25). For instance, in the sediment of Lake Washington methane-utilizing communities are not random; they are dominated by methanotrophs within the family Methylococcaceae and nonmethanotrophic methylotrophs within the family Methylophilaceae and also include other specific non-methane-utilizing heterotrophs (18,19).…”

mentioning

confidence: 99%

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

Krause

Johnson

Karunaratne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

147

144

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The utilization of methane, a potent greenhouse gas, is an important component of local and global carbon cycles that is characterized by tight linkages between methane-utilizing (methanotrophic) and nonmethanotrophic bacteria. It has been suggested that the methanotroph sustains these nonmethanotrophs by cross-feeding, because subsequent products of the methane oxidation pathway, such as methanol, represent alternative carbon sources. We established cocultures in a microcosm model system to determine the mechanism and substrate that underlay the observed cross-feeding in the environment. Lanthanum, a rare earth element, was applied because of its increasing importance in methylotrophy. We used co-occurring strains isolated from Lake Washington sediment that are involved in methane utilization: a methanotroph and two nonmethanotrophic methylotrophs. Gene-expression profiles and mutant analyses suggest that methanol is the dominant carbon and energy source the methanotroph provides to support growth of the nonmethanotrophs. However, in the presence of the nonmethanotroph, gene expression of the dominant methanol dehydrogenase (MDH) shifts from the lanthanide-dependent MDH (XoxF)-type, to the calcium-dependent MDH (MxaF)-type. Correspondingly, methanol is released into the medium only when the methanotroph expresses the MxaF-type MDH. These results suggest a cross-feeding mechanism in which the nonmethanotrophic partner induces a change in expression of methanotroph MDHs, resulting in release of methanol for its growth. This partner-induced change in gene expression that benefits the partner is a paradigm for microbial interactions that cannot be observed in studies of pure cultures, underscoring the importance of synthetic microbial community approaches to understand environmental microbiomes. M icrobial communities and their members are part of every ecosystem and drive important biogeochemical processes on Earth (1). They typically comprise a range of phylogenetically and functionally diverse microbes (2) that are structured by biotic and abiotic factors (3) and are entangled through specific interactions in complex networks (4).The significance of microbial communities in diverse ecosystems including the human body is now widely accepted in science and has led to a range of initiatives focused on the world's microbiomes (5, 6). One important goal within these efforts is to understand how microbes interact with each other and the consequences of such interactions at the level of their transcriptomes, proteomes, and metabolomes. For instance, it has been demonstrated that the metabolism of yeast can be transformed by bacteria-induced prions to decrease the release of inhibiting ethanol (7). In another study, an oral biofilm of the genus Streptococcus displayed different transcriptional responses toward the presence of other species in mixed-species cultures (8).Measuring interactions in complex environmental communities is still a difficult task. Laboratory cocultures represent a simplified approach to assessing...

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Methane assimilation and trophic interactions with marine Methylomicrobium in deep-water coral reef sediment off the coast of Norway

Cited by 43 publications

References 59 publications

Response to Comment on “A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico”

Response to Comment on “A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico”

Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill

Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions

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